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Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation
Microorganisms require efficient translation to grow and replicate rapidly, and translation is often rate-limited by initiation. A prominent feature that facilitates translation initiation in bacteria is the Shine–Dalgarno (SD) sequence. However, there is much debate over its conservation in Cyanoba...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6847405/ https://www.ncbi.nlm.nih.gov/pubmed/31621842 http://dx.doi.org/10.1093/gbe/evz227 |
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author | Wei, Yulong Xia, Xuhua |
author_facet | Wei, Yulong Xia, Xuhua |
author_sort | Wei, Yulong |
collection | PubMed |
description | Microorganisms require efficient translation to grow and replicate rapidly, and translation is often rate-limited by initiation. A prominent feature that facilitates translation initiation in bacteria is the Shine–Dalgarno (SD) sequence. However, there is much debate over its conservation in Cyanobacteria and in chloroplasts which presumably originated from endosymbiosis of ancient Cyanobacteria. Elucidating the utilization of SD sequences in Cyanobacteria and in chloroplasts is therefore important to understand whether 1) SD role in Cyanobacterial translation has been reduced prior to chloroplast endosymbiosis or 2) translation in Cyanobacteria and in plastid has been subjected to different evolutionary pressures. To test these alternatives, we employed genomic, proteomic, and transcriptomic data to trace differences in SD usage among Synechocystis species, Microcystis aeruginosa, cyanophages, Nicotiana tabacum chloroplast, and Arabidopsis thaliana chloroplast. We corrected their mis-annotated 16S rRNA 3′ terminus using an RNA-Seq-based approach to determine their SD/anti-SD locational constraints using an improved measurement D(toStart). We found that cyanophages well-mimic Cyanobacteria in SD usage because both have been under the same selection pressure for SD-mediated initiation. Whereas chloroplasts lost this similarity because the need for SD-facilitated initiation has been reduced in plastids having much reduced genome size and different ribosomal proteins as a result of host-symbiont coevolution. Consequently, SD sequence significantly increases protein expression in Cyanobacteria but not in chloroplasts, and only Cyanobacterial genes compensate for a lack of SD sequence by having weaker secondary structures at the 5′ UTR. Our results suggest different evolutionary pressures operate on translation initiation in Cyanobacteria and in chloroplast. |
format | Online Article Text |
id | pubmed-6847405 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-68474052019-11-15 Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation Wei, Yulong Xia, Xuhua Genome Biol Evol Research Article Microorganisms require efficient translation to grow and replicate rapidly, and translation is often rate-limited by initiation. A prominent feature that facilitates translation initiation in bacteria is the Shine–Dalgarno (SD) sequence. However, there is much debate over its conservation in Cyanobacteria and in chloroplasts which presumably originated from endosymbiosis of ancient Cyanobacteria. Elucidating the utilization of SD sequences in Cyanobacteria and in chloroplasts is therefore important to understand whether 1) SD role in Cyanobacterial translation has been reduced prior to chloroplast endosymbiosis or 2) translation in Cyanobacteria and in plastid has been subjected to different evolutionary pressures. To test these alternatives, we employed genomic, proteomic, and transcriptomic data to trace differences in SD usage among Synechocystis species, Microcystis aeruginosa, cyanophages, Nicotiana tabacum chloroplast, and Arabidopsis thaliana chloroplast. We corrected their mis-annotated 16S rRNA 3′ terminus using an RNA-Seq-based approach to determine their SD/anti-SD locational constraints using an improved measurement D(toStart). We found that cyanophages well-mimic Cyanobacteria in SD usage because both have been under the same selection pressure for SD-mediated initiation. Whereas chloroplasts lost this similarity because the need for SD-facilitated initiation has been reduced in plastids having much reduced genome size and different ribosomal proteins as a result of host-symbiont coevolution. Consequently, SD sequence significantly increases protein expression in Cyanobacteria but not in chloroplasts, and only Cyanobacterial genes compensate for a lack of SD sequence by having weaker secondary structures at the 5′ UTR. Our results suggest different evolutionary pressures operate on translation initiation in Cyanobacteria and in chloroplast. Oxford University Press 2019-10-22 /pmc/articles/PMC6847405/ /pubmed/31621842 http://dx.doi.org/10.1093/gbe/evz227 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Article Wei, Yulong Xia, Xuhua Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation |
title | Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation |
title_full | Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation |
title_fullStr | Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation |
title_full_unstemmed | Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation |
title_short | Unique Shine–Dalgarno Sequences in Cyanobacteria and Chloroplasts Reveal Evolutionary Differences in Their Translation Initiation |
title_sort | unique shine–dalgarno sequences in cyanobacteria and chloroplasts reveal evolutionary differences in their translation initiation |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6847405/ https://www.ncbi.nlm.nih.gov/pubmed/31621842 http://dx.doi.org/10.1093/gbe/evz227 |
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